Salt stress affects mRNA editing in soybean chloroplasts

Abstract Soybean, a crop known by its economic and nutritional importance, has been the subject of several studies that assess the impact and the effective plant responses to abiotic stresses. Salt stress is one of the main environmental stresses and negatively impacts crop growth and yield. In this work, the RNA editing process in the chloroplast of soybean plants was evaluated in response to a salt stress. Bioinformatics approach using sRNA and mRNA libraries were employed to detect specific sites showing differences in editing efficiency. RT-qPCR was used to measure editing efficiency at selected sites. We observed that transcripts of NDHA, NDHB, RPS14 and RPS16 genes presented differences in coverage and editing rates between control and salt-treated libraries. RT-qPCR assays demonstrated an increase in editing efficiency of selected genes. The salt stress enhanced the RNA editing process in transcripts, indicating responses to components of the electron transfer chain, photosystem and translation complexes. These increases can be a response to keep the homeostasis of chloroplast protein functions in response to salt stress.

[1]  Congming Lu,et al.  LPA66 Is Required for Editing psbF Chloroplast Transcripts in Arabidopsis1[W][OA] , 2009, Plant Physiology.

[2]  D. Jiang,et al.  Increasing cyclic electron flow is related to Na+ sequestration into vacuoles for salt tolerance in soybean , 2015, Journal of experimental botany.

[3]  Maki Yukawa,et al.  A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. , 2004, Plant & cell physiology.

[4]  C. Schmitz-Linneweber,et al.  Short non-coding RNA fragments accumulating in chloroplasts: footprints of RNA binding proteins? , 2011, Nucleic acids research.

[5]  Sandra K. Tanz,et al.  AEF1/MPR25 is implicated in RNA editing of plastid atpF and mitochondrial nad5, and also promotes atpF splicing in Arabidopsis and rice. , 2015, The Plant journal : for cell and molecular biology.

[6]  D. Jiang,et al.  Induction of cyclic electron flow around photosystem 1 and state transition are correlated with salt tolerance in soybean , 2008, Photosynthetica.

[7]  N. Tuteja,et al.  Cold, salinity and drought stresses: an overview. , 2005, Archives of biochemistry and biophysics.

[8]  R. Bock,et al.  The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins. , 2012, The Plant journal : for cell and molecular biology.

[9]  I. Small,et al.  The PPR motif - a TPR-related motif prevalent in plant organellar proteins. , 2000, Trends in biochemical sciences.

[10]  E. Olmos,et al.  Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. , 2003, Journal of experimental botany.

[11]  W. Huber,et al.  Differential expression analysis for sequence count data , 2010 .

[12]  I. Small,et al.  A rapid high-throughput method for the detection and quantification of RNA editing based on high-resolution melting of amplicons , 2007, Nucleic acids research.

[13]  A. Barkan,et al.  Pentatricopeptide repeat proteins in plants. , 2014, Annual review of plant biology.

[14]  Ian Small,et al.  The cytidine deaminase signature HxE(x)n CxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. , 2014, The New phytologist.

[15]  M. Williams,et al.  Incomplete editing of rps12 transcripts results in the synthesis of polymorphic polypeptides in plant mitochondria. , 1996, The Plant cell.

[16]  T. Shikanai,et al.  Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. , 2011, Biochimica et biophysica acta.

[17]  A. Barkan,et al.  Protein-mediated protection as the predominant mechanism for defining processed mRNA termini in land plant chloroplasts , 2011, Nucleic acids research.

[18]  Michael Mulligan,et al.  Heat stress results in incomplete C-to-U editing of maize chloroplast mRNAs and correlates with changes in chloroplast transcription rate , 2001, Current Genetics.

[19]  M. Hanson,et al.  Cytidine Deaminase Motifs within the DYW Domain of Two Pentatricopeptide Repeat-containing Proteins Are Required for Site-specific Chloroplast RNA Editing* , 2014, The Journal of Biological Chemistry.

[20]  Takahiro J. Nakamura,et al.  Pentatricopeptide repeat proteins involved in plant organellar RNA editing , 2013, RNA biology.

[21]  A. Das,et al.  Salt tolerance and salinity effects on plants: a review. , 2005, Ecotoxicology and environmental safety.

[22]  Axel Brennicke,et al.  RNA editing in plants and its evolution. , 2013, Annual review of genetics.

[23]  P. Dix,et al.  Variations in efficiency of plastidial RNA editing within ndh transcripts of perennial ryegrass (Lolium perenne) are not linked to differences in drought tolerance , 2013, AoB Plants.

[24]  R. Vaňková,et al.  Abscisic acid represses the transcription of chloroplast genes* , 2013, Journal of experimental botany.

[25]  G. Garab,et al.  The effects of salt stress on photosynthetic electron transport and thylakoid membrane proteins in the cyanobacterium Spirulina platensis. , 2005, Journal of biochemistry and molecular biology.

[26]  H. Koyro Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.) , 2006 .

[27]  Jeffrey P. Mower The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments , 2009, Nucleic Acids Res..

[28]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[29]  Frédérique Bitton,et al.  Genome-Wide Analysis of Arabidopsis Pentatricopeptide Repeat Proteins Reveals Their Essential Role in Organelle Biogenesis , 2004, The Plant Cell Online.

[30]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[31]  W. Chow,et al.  A real-time PCR method for the quantitative analysis of RNA editing at specific sites. , 2008, Analytical biochemistry.

[32]  A. Barkan Expression of Plastid Genes: Organelle-Specific Elaborations on a Prokaryotic Scaffold1 , 2011, Plant Physiology.

[33]  R. Oelmüller,et al.  Expression of the ribosomal proteins S14, S16, L13a and L30 is regulated by cytokinin and abscisic acid: Implication of the involvement of phytohormones in translational processes , 2003 .

[34]  T. Kakizaki,et al.  Plastid signalling under multiple conditions is accompanied by a common defect in RNA editing in plastids , 2011, Journal of experimental botany.

[35]  D. Karcher,et al.  Temperature sensitivity of RNA editing and intron splicing reactions in the plastid ndhB transcript , 2002, Current Genetics.

[36]  Bartolomé Sabater,et al.  Plastid ndh genes in plant evolution. , 2010, Plant physiology and biochemistry : PPB.

[37]  Mitsuyasu Hasebe,et al.  High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. , 2004, Gene.

[38]  Stefan A. Rensing,et al.  RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal , 2009, Molecular Genetics and Genomics.

[39]  W. Cao,et al.  Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. , 2009, Plant science : an international journal of experimental plant biology.

[40]  I. Small,et al.  Organellar RNA editing , 2011, Wiley interdisciplinary reviews. RNA.

[41]  Ian Small,et al.  Plant RNA editing , 2010, RNA biology.

[42]  A. Araya,et al.  RNA editing in plant organelles. Why make it easy? , 2011, Biochemistry (Moscow).

[43]  A. Altman,et al.  Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance , 2003, Planta.

[44]  S. Allakhverdiev,et al.  Photoinhibition of photosystem II under environmental stress. , 2007, Biochimica et biophysica acta.

[45]  M. Hsieh,et al.  Differential regulation of Arabidopsis plastid gene expression and RNA editing in non-photosynthetic tissues , 2013, Plant Molecular Biology.

[46]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[47]  Kim N Dang,et al.  A Conserved Glutamate Residue in the C-terminal Deaminase Domain of Pentatricopeptide Repeat Proteins Is Required for RNA Editing Activity* , 2015, The Journal of Biological Chemistry.

[48]  K. Shinozaki,et al.  Differential Gene Expression in Soybean Leaf Tissues at Late Developmental Stages under Drought Stress Revealed by Genome-Wide Transcriptome Analysis , 2012, PloS one.

[49]  Pablo Vera,et al.  Mediated Plastid RNA Editing in Plant Immunity , 2013, PLoS pathogens.

[50]  A. Brennicke,et al.  The process of RNA editing in plant mitochondria. , 2008, Mitochondrion.

[51]  K. Shinozaki,et al.  Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[52]  A. Moorman,et al.  Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data , 2009, Nucleic acids research.

[53]  Jiang Zhang,et al.  Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco , 2008, Plant Cell Reports.